Geographic Variation in Photoperiodic Response for Induction of Pseudopupal Diapause in Epicauta gorhami (Coleoptera: Meloidae)
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Environmental Entomology, 50(5), 2021, 1145–1150
doi: 10.1093/ee/nvab062
Advance Access Publication Date: 25 June 2021
Research
Physiological Ecology
Geographic Variation in Photoperiodic Response for
Induction of Pseudopupal Diapause in Epicauta gorhami
(Coleoptera: Meloidae)
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Misato Terao,1,2 Makoto Tokuda,1,3 and Yoshinori Shintani4,5,
1
The United Graduate School of Agricultural Sciences, Kagoshima University, Kagoshima 890-0065, Japan, 2Field Center,
Department of Environmental and Horticultural Sciences, Minami Kyushu University, 3764-1 Tateno, Miyakonojo, Miyazaki 885-0035,
Japan, 3Laboratory of Systems Ecology, Faculty of Agriculture, Saga University, Saga 840–8502, Japan, 4Laboratory of Entomology,
Department of Environmental and Horticultural Sciences, Minami Kyushu University, 3764-1 Tateno, Miyakonojo, Miyazaki 885-0035,
Japan, and 5Corresponding author, e-mail: shintani@nankyudai.ac.jp
Subject Editor: Colin Brent
Received 6 March 2021; Editorial decision 29 May 2021
Abstract
Geographical variations in the threshold of environmental cues for diapause induction are important in understanding
the life history strategy of insects. Larvae of the bean blister beetle, Epicauta gorhami (Coleoptera: Meloidae), feed
on grasshopper eggs and undergo hypermetamorphosis. They normally enter diapause as a pseudopupa (fifth
instar). However, when the larvae are reared under long-day and high-temperature conditions, they do not enter
pseudopupal diapause but pupate directly from the fourth instar. In addition, this insect is known to modify its
photoperiodic response for induction of pseudopupal diapause depending on food availability for larvae. In this
study, the larval photoperiodic responses for diapause induction were examined for three populations of E. gorhami
collected from the northernmost (Morioka, 39.7°N), central (Kazo, 36.1°N), and southernmost (Takanabe, 32.1°N) parts
of its distribution range, and the responses were examined under both fully fed and food-deprived (FD) conditions.
Diapause incidence decreased in FD larvae for all populations in long-day conditions, and the critical day-lengths for
the diapause incidence were calculated as 14.81, 13.97, and 13.99 h in the Morioka, Kazo, and Takanabe populations,
respectively.The results indicate the presence of a geographical variation in larval photoperiodic response, in which
diapause is induced earlier in higher latitudinal areas. From these results, together with data for developmental
threshold temperature and thermal constant, the Morioka and Kazo populations were suggested to have a partial
bivoltine life cycle under the conditions of extremely early oviposition season, a sufficient summer temperature,
and poor larval food availability.
Key words: hypermetamorphosis, precocious metamorphosis, pseudopupal diapause, seasonal adaptation, voltinism
Insects have adapted to various seasonally changing environments. life history strategy, environmental adaptation, and ecological sig-
To survive seasons unsuitable for growth and reproduction, many nificance of diapause in insects.
insects enter diapause by responding to environmental cues such as The bean blister beetle, Epicauta gorhami Marseul (Coleoptera:
temperature and photoperiod. Reflecting the diverse life histories of Meloidae), is distributed in a wide latitudinal range in Japan from
insects, diapause traits also exhibit large variations in terms of de- Honshu to Kyushu Islands (Mochida 2003). The adults are polypha-
velopmental stages and seasons in which diapause occurs, as well as gous herbivores associated with various crops and wild herbaceous
the length of the diapause period and requisites of diapause induc- plants, whereas larvae feed only on grasshopper eggs and develop in
tion and termination (Tauber et al. 1986, Danks 1987, Kostál 2006). grasshopper egg pods laid in soil. The species has a unique develop-
Geographical variations in the threshold of environmental cues for mental process in the larval stage; i.e., the larvae undergo hypermet-
diapause induction are particularly important in understanding the amorphosis, which is characteristic to meloid beetles.
Published by Oxford University Press on behalf of Entomological Society of America 2021. This work is
written by (a) US Government employee(s) and is in the public domain in the US.
11451146 Environmental Entomology, 2021, Vol. 50, No. 5
Hypermetamorphosis is a form of holometabolism through increases. This is because the period suitable for growth and repro-
which the larval shape drastically changes at the larval-larval ec- duction is shorter at higher latitudes and longer at low latitudes,
dysis. Meloid larvae have four distinctive phases in the process of and insects have evolved geographically different seasonal life cycles
hypermetamorphosis: the planidium, first grub, coarctate (pseudop- as adaptations to the environments of their habitats (Danilevskii
upa), and second grub stages (Balduf 1935, Clausen 1940, Selander 1965, Tauber et al. 1986). However, geographic variations in photo-
and Mathieu 1964, Pinto 2009). In E. gorhami, the planidia (first periodic response have yet to be examined for meloid beetles, pos-
instar) forage for food resources and burrow into a grasshopper egg sibly because of the difficulty in mass-rearing these beetles in the
pod. First grubs (second to fourth instars) are less mobile and cannot laboratory.
find another egg pod when the food is exhausted. Thus, the larval In the present study, feeding status-dependent photoperiodic
food resources for completion of development are limited to the egg responses were examined for three geographical populations of
pod into which the planidia first burrow. In fact, the larvae have E. gorhami collected from different latitudes. The developmental
the ability to metamorphose to pupae or pseudopupae without fur- threshold temperature and thermal constant of the three popula-
ther feeding if they reach fourth instar, as described below. In add- tions were also investigated and voltinism is discussed based on the
ition, there is a large variation in body size in field-collected adults, climate data for each population.
Downloaded from https://academic.oup.com/ee/article/50/5/1145/6309171 by guest on 03 November 2021
which suggests an individual variation in food availability in the
larval stage (Terao, unpublished data). The pseudopupa (fifth instar
in E. gorhami) is a characteristic form of hypermetamorphosis in Materials and Methods
meloid beetles and serves as a dormant stage in the family.
Insects
Larval development of E. gorhami is controlled by temperature
Adults of E. gorhami were collected from grassland or cropland at
and photoperiod: at low temperatures (≤22.5°C) all larvae enter
three sites in Japan: Morioka (39.7°N, 141.2°E), Iwate Prefecture;
pseudopupal diapause and at moderate temperatures (around 25°C)
Kazo (36.1°N, 139.6°E), Saitama Prefecture; and Takanabe (32.1°N,
all larvae enter pseudopupal diapause under short-day conditions,
131.5°E), Miyazaki Prefecture, from summer to autumn in 2016 to
whereas a few larvae directly pupate from the fourth instar under
2019 (Fig. 2). They were placed individually or in female-male pairs
long-day conditions (Shintani et al. 2011). Thus, the photoperiodic
in 200 ml plastic cups with moistened sand (ca. 6 wt% water con-
response curve is not clear and at high temperatures (≥27.5°C) most
tent and 1.5 cm depth) to obtain eggs. Egg masses deposited in the
larvae pupate directly from the fourth instar regardless of the photo-
sand were placed on slightly moistened paper towel in plastic Petri
periodic conditions (Shintani et al. 2011). In addition, we have found
dishes (6 cm diameter) and kept at 25°C under LD 16:8 h (16-hour
that food availability, which varies depending on the size of the egg
light and 8-hour dark) until hatching. Newly hatched larvae were
pods into which the first instar larvae burrow, also affects larval de-
placed individually into plastic Petri dishes (6 cm diameter) with a
velopment of E. gorhami (Terao et al. 2015). At 25°C, all larvae
piece of an egg pod of the migratory locust, Locusta migratoria (L.)
supplied with enough food entered pseudopupal diapause, whereas
(Orthoptera: Acrididae) as food for the E. gorhami larvae. The egg
some larvae deprived of food at the fourth instar pupated without
pods were obtained from greenhouse-reared grasshoppers originat-
diapause even under short-day conditions, and as a result, diapause
ing from the field. The rearing methods were based on our previous
incidence was generally lower. These food-deprived (FD) fourth-in-
studies (Shintani et al. 2011, Terao et al. 2012, 2015).
star larvae pupate or pseudopupate earlier with smaller body sizes
(precocious metamorphosis) compared to those supplied with
enough food. As a result, the photoperiodic response curve became Feeding Conditions and Photoperiodic Response
clearer and the critical day-length shortened in FD larvae. A study Larvae of the three populations were reared from hatching at 25°C
performed outdoors showed that such larval responses to environ- under five different photoperiodic conditions (LD 12:12, 13:11,
mental conditions affect the voltinism of E. gorhami (Shintani et al. 14:10, 15:9, and 16:8 h). Two feeding treatments (‘FD’ and ‘fully fed
2017). The seasonal life cycle of E. gorhami in southern Japan is (FF)’) were used for each photoperiodic condition. In FD treatment,
shown in Fig. 1. larvae were observed for their instar by slitting the food (pieces of
The photoperiodic response for diapause induction in many in- grasshopper egg pod). Newly-ecdysed fourth-instar larvae obtained
sects varies geographically as a result of adaptation to the climate of by observation performed three times a day in the beginning, middle,
the habitat (Masaki 1961, Tauber and Tauber 1972, Shintani et al. and terminal periods of the photophase were taken out to determine
1996, Gomi 1997). Such variations are important information in their body weight. Larvae of body weight 50–65 mg (within 24 h
understanding survival strategies in insects. In general, the critical after the ecdysis) were deprived of food and transferred to another
day-length for diapause induction becomes longer as the latitude Petri dish containing only slightly moistened paper towel. Other
Fig. 1. Schematic drawing of the seasonal life cycle of Epicauta gorhami in southern Japan (inferred from Shintani et al. 2011, 2017, Terao et al. 2012, 2015). The
beetle exhibits a partially bivoltine life cycle.Environmental Entomology, 2021, Vol. 50, No. 5 1147
larvae, including those of body weight >65 mg, were fed additional by keeping the pupae under the same temperature and photoperiod
pieces of grasshopper egg pods and used for FF treatment. In this conditions (25, 27.5, and 30°C, under LD 16:8 h). Data for the larval
way, larvae were assigned to FD or FF treatment groups. and pupal period were analyzed to calculate T0 and K according to
Ikemoto and Takai (2000). In FD larvae, K is obtained by calculating
Developmental Threshold Temperature and Thermal coefficients from the data of FF larval period at 25°C, assuming that
Constant in the Egg, Larval, and Pupal Stages T0 is not different between FD and FF larvae.
The eggs of three populations kept at 25°C under LD 16:8 h and
their egg periods were investigated. The egg periods were approxi- Statistical Analysis
mately the same in all populations. Therefore, as the developmental Diapause incidences was compared among populations using Fisher
threshold temperature (T0) and thermal constant (K) of the eggs for exact test. P values were adjusted by Holm’s sequential correction
all three populations, those for the Takanabe population (Shintani method. Critical photoperiod for diapause induction was calculated
et al. 2011) were used. To compare larval developmental parameters using logistic regression analysis.
among the three populations, larvae were reared individually from
hatching at six temperatures (17.5, 20, 22.5, 25, 27.5, and 30°C)
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Climatic Data
under LD 16:8 h and their larval periods were investigated. Pupal
developmental parameters for the three populations were obtained To examine the seasonal development of E. gorhami larvae, data
for temperatures (2010–2019) and day-length at the three collection
sites were obtained from the Japan Meteorological Agency (2020)
and Time and Date AS (2019), respectively. The day-length includes
twilight.
Results
Geographic Variation in Photoperiodic Responses
for Pseudopupal Diapause Induction
The photoperiodic responses for pseudopupal diapause induc-
tion in E. gorhami larvae are shown in Fig. 3. With FF treatment,
diapause incidence tended to be higher under short-day condi-
tions, but the response was unclear in all populations. Individuals
entered diapause under LD 12:12 h, while diapause incidence
varied under LD 16:8 h, with rates of 78.1, 36.0, and 57.7% in
the Morioka, Kazo, and Takanabe populations, respectively (Fig.
3a). With FD treatment, however, the photoperiodic response
was clearer in all populations. The diapause incidences under
LD 12:12 h were 82.8–100% in the three populations and de-
creased markedly with an increase in photoperiod, with rates of
10.3, 7.4, and 18.8% under LD 16:8 h in the respective popula-
tions (Fig. 3b). Geographic variation was detected in the photo-
periodic response of FD larvae, with diapause incidences differing
significantly among the populations. For example, those under
LD 14:10 h were 96.6, 66.7, and 30.3% in the Morioka, Kazo,
Fig. 2. Collection sites of Epicauta gorhami. and Takanabe populations. The critical day-lengths for diapause
Fig. 3. Comparison of photoperiodic response among three populations of Epicauta gorhami under (a) FF and (b) FD conditions. Larvae were reared from
hatching under different photoperiodic conditions at 25°C. Larvae were FF or FD on the day of ecdysis to the fourth instar. The sample size was 21–34 for each
group. Values with the same letter did not differ significantly (P > 0.05; Fisher exact test among populations within the same photoperiod; P values were adjusted
by Holm’s sequential correction method).1148 Environmental Entomology, 2021, Vol. 50, No. 5
Table 1. Larval period in days (mean ± SD) at various temperatures under LD 16:8 h and estimated developmental threshold temperature
(T0) and thermal constant (K) in three populations of Epicauta gorhami under the FF conditiona
Temperature Pupa-destinedc Pseudopupa-destinedc
(°C)
Morioka Kazo Takanabe Morioka Kazo Takanabe
17.5 – – – 38.4 ± 3.1 (27) 39.3 ± 4.6 (28) 43.4 ± 5.3 (29)
20 – – – 29.8 ± 2.3 (29) 35.5 ± 3.7 (24) 36.0 ± 5.0 (28)
22.5 – – – 25.2 ± 3.2 (27) 28.9 ± 3.2 (29) 28.8 ± 3.4 (33)
25 24.2 ± 2.0 (6) 23.0 ± 1.4 (15) 24.3 ± 1.4 (11) 18.5 ± 2.2 (25) 22.0 ± 2.6 (9) 23.5 ± 1.6 (15)
27.5 17.7 ± 1.5 (29) 19.8 ± 2.1 (25) 20.7 ±1.8 (27) 17.0 ± 1.0 (6) 22.5 ± 3.5 (2)b 21.0 ± 1.8 (6)
30 15.7 ± 2.1 (28) 17.5 ± 2.2 (32) 17.7 ±1.7 (27) – – –
T0 (°C) 16.3 9.0 11.5 10.1 8.5 8.7
K (degree-days) 207.2 367.3 329.0 293.4 381.7 392.7
r2 0.9867 0.9983 0.9969 0.9758 0.8391 0.9848
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a
Until pupation or pseudopupation.
b
Not used for estimation of developmental parameters due to the small sample size.
c
Numbers in parentheses indicate sample size.
induction of 14.81, 13.97, and 13.99 h also differed among the Table 2. Thermal constant (degree-days) of Epicauta gorhami lar-
respective populations. vae under the FD condition
Morioka Kazo Takanabe
Developmental Threshold Temperature and Thermal
Constant Pupa-destined 152.0 298.3 258.6
The estimated threshold temperature (T0) and thermal constant Pseudopupa-destined 222.3 305.4 311.5
(K) for the larval stage calculated from larval durations are shown
in Table 1. The threshold temperatures of the Morioka, Kazo, and Values were obtained as products of the thermal constant under the FF con-
dition and the larval duration under the FD condition relative to that under
Takanabe populations were estimated to be 16.3, 9.0, and 11.5°C
the FF condition at 25°C (0.734–0.812).
for pupa-destined larvae and 10.1, 8.5, and 8.7°C for pseudop-
upa-destined larvae. The estimated thermal constants of the re-
which was used as the southernmost site in the present study.
spective populations were 207.2, 367.3, and 329.0 degree-days for
A previous study (Shintani et al. 2017) showed that the Takanabe
pupa-destined larvae and 293.4, 381.7, and 392.7 degree-days for
population of E. gorhami partially becomes bivoltine. Here,
pseudopupa-destined larvae. These parameters for other develop-
the possibility of partial bivoltine life cycle in more northern
mental stages are shown in Table 2. In the eggs of the three popu-
areas (Morioka and Kazo) is assessed using the developmental
lations, the estimated threshold temperature and thermal constant
threshold temperature and thermal constant. In addition, food
are 14.2°C and 166.9 degree-days. These developmental data of
shortage during the larval period induces premature pupation,
eggs were referred from the previous study (Shintani et al. 2011).
which results in shortening of the larval duration and an increase
In the pupal stage, the threshold temperatures of the Morioka,
of pupation rates (Terao et al. 2015). Considering such effects
Kazo, and Takanabe populations were estimated to be 10.6, 10.7,
of premature pupation, we estimated the number of generations
and 13.3°C. The estimated thermal constants of the respective
per year under food shortage conditions using the thermal con-
populations were 141.4, 146.7, and 130.6 degree-days (Table 3).
stants shown in Tables 2 and 3. Larvae of all populations were
assumed to hatch on 1 August, which is 6–10 d earlier than the
hatching date for the bivoltine life cycle in the Takanabe popula-
Discussion tion (Shintani et al. 2017). The estimated developmental progress
In this study, larval photoperiodic responses for diapause induction is shown in Fig. 4.
are compared in three populations of E. gorhami, including those In the Morioka population, next-generation (first generation
collected from the northernmost to southernmost distribution areas, of the year) adults were estimated to appear on 28 August under
under two feeding conditions. Under long-day conditions, diapause a food shortage and on 6 September with sufficient food. Even if
incidence decreased in FD larvae in all populations. Critical day- these adults oviposited in the same year, the eggs cannot hatch due
lengths for diapause were 14.81, 13.97, and 13.99 h in the Morioka, to the limit on thermal accumulation. Therefore, if eggs laid by
Kazo, and Takanabe populations, respectively. This result indicates a overwintered adults hatched on 1 August, this hatched generation
geographical variation in the photoperiodic response in E. gorhami cannot reach the diapause stage. However, for eggs laid in early sea-
larvae, in which the larval diapause of E. gorhami is induced earlier sons and if the air temperature of the focal year was higher than
at higher latitudes. usual, a partial population might exhibit bivoltine life cycles because
In general, intraspecies differences in the threshold tempera- a geographical variation was detected in the photoperiodic response
ture are not large (Kiritani 2012). However, the results of this study of diapause induction in this study; thus, the response may function
showed large differences in the threshold temperature between the as phenotypic plasticity. The exact season of adult emergence was
geographical populations of E. gorhami, although the reason is not clarified in the Morioka population, but a bivoltine life cycle
not clear. may be possible under a food shortage for eggs hatched on 26 July
According to our preliminary observations, adults of and a summer temperature as high as that in 2010, when the mean
E. gorhami are found from mid-July to early October in Takanabe, summer temperature was the highest in the past 20 yr. Furthermore,Environmental Entomology, 2021, Vol. 50, No. 5 1149
Table 3. Developmental period in days (mean ± SD) at three temperatures under LD 16:8 h and estimated developmental parameters of the
egg and pupal stages in the three populations of Epicauta gorhami
Temperature (°C) Eggd Pupabd
Population Population
Morioka Kazo Takanabe Morioka Kazo Takanabe
25 15.3 ± 0.6 (11) 15.6 ± 0.7 (8) 15.8 ± 0.4 (6) 9.8 ± 0.4 (5) 10.2 ± 0.4 (14) 11.2 ± 0.4 (11)
27.5 – – – 8.3 ± 0.6 (29) 8.8 ± 0.4 (24) 9.0 ± 0.3 (26)
30 – – – 7.3 ± 0.7 (28) 7.6 ± 0.5 (32) 7.9 ± 0.3 (27)
T0 (°C) 14.2a 10.6 10.7 13.3
K (degree-days) 166.9a 141.4 146.7 130.6
r2 0.997a 0.9988 0.9907 0.9914
K (degree-days) – – – 133.2 137.8 113.4
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premature pupationc
a
Data shown in Shintani et al. (2011) were used for the developmental threshold temperature and thermal constant of the egg stage because the egg periods at
25°C are fundamentally the same in the three populations.
b
Pupal periods under FF conditions were used for the three populations.
c
Values were estimated from the duration of pupae derived from FD larvae, assuming that T0 is not variable depending on the larval food condition.
d
Numbers in parentheses indicate sample size.
Fig. 4. Schematic representation of the developmental progress of Epicauta gorhami estimated from the results of this study and seasonal changes in mean air
temperature at the three sites. The larvae of all populations are assumed to hatch on 1 August. Open triangles show the estimated times of adult emergence.
Closed triangles show the estimated times when the next-generation larvae reach the pseudopupal stage. The double arrow shows the period in which the next
generation of the Takanabe population reached the pseudopupal stage under outdoor conditions (Shintani et al. 2017). The broken lines on the bars represent
the critical day-length for induction of pseudopupal diapause under the food-deprived condition at 25°C. Temperatures are shown as the daily average from 2010
to 2019. The day-length includes twilight.
larvae that hatch on 26 July are estimated to pupate on 10 August. population, regardless of feeding conditions. In a food shortage,
Because the critical day-length for diapause induction (14.81 h) falls larvae are assumed to reach pseudopupal diapause on 17 October. In
around 13 August (Fig. 4), non-diapause individuals may possibly contrast, with sufficient food, the larval duration of the next gener-
appear in the field. ation should become longer due to the rapid decrease in temperature
In the Kazo population, next-generation adults are estimated to from mid-September and pseudopupal diapause should be reached
appear and oviposit at about the same time as that in the Takanabe in mid-November. However, the temperature is sometimes below the1150 Environmental Entomology, 2021, Vol. 50, No. 5
developmental threshold temperature in November and it is uncer- Gomi, T. 1997. Geographic variation in critical photoperiod for diapause
tain if larvae can survive until the pseudopupae stage. induction and its temperature dependence in Hyphantria cunea Drury
These estimations suggest that the Morioka and Kazo popu- (Lepidoptera: Arctiidae). Oecologia. 111: 160–165.
Ikemoto, T., and K. Takai. 2000. A new linearized formula for the law of total
lations have the possibility of a partial bivoltine life cycle, if their
effective temperature and the evaluation of line-fitting methods with both
oviposition season is early and the summer temperature is suffi-
variables subject to error. Environ. Entomol. 29: 671–682.
ciently high. In addition, the Morioka population has a higher de-
Kiritani, K. 2012. The low development threshold temperature and the
velopmental threshold temperature and a smaller thermal constant thermal constant in insects and mites in Japan. 2nd ed. Bull. Natn. Inst.
in the larval period compared to the other two populations. This Agro-Environ. Sci. 31: 1–74 (in Japanese with English abstract).
trait probably plays a role in completing growth and reproduction Kostál, V. 2006. Eco-physiological phases of insect diapause. J. Insect Physiol.
within the relatively short suitable season in Morioka. Otherwise, if 52: 113–127.
larvae of the Morioka population encounter a food shortage, prema- Masaki, S. 1961. Geographic variation of diapause in insects. Bull. Fac. Agric.
ture metamorphosis will increase their pupation rate and shorten the Hirosaki Univ. 7: 66–98.
larval period. Therefore, the population might partially exhibit the Matsuda, N., K. Tanaka, Y. Watari, Y. Shintani, S. G. Goto, T. Nisimura,
Y. Izumi, and H. Numata. 2018. Northward expansion of the bivoltine
bivoltine life cycle, as in the Takanabe population.
Downloaded from https://academic.oup.com/ee/article/50/5/1145/6309171 by guest on 03 November 2021
life cycle of the cricket over the last four decades. Glob. Chang. Biol. 24:
The results of this study showed that the Morioka population,
5622–5628.
which was collected from the northernmost part of the distribution
Mochida, O. 2003. Epicauta gorhami Marseul, pp. 164–165. In K. Umeya
range, also retains phenotypic plasticity in diapause induction. The rise and T. Okada (eds.), Agricultural Insect Pests in Japan. Zenkoku Noson
of temperature due to recent global warming has had a major impact Kyoiku Kyokai, Tokyo (in Japanese).
on organisms, including insects (Parmesan 2006, Andrew et al. 2013, Parmesan, C. 2006. Ecological and evolutionary responses to recent climate
Boukal et al. 2019). One of the important effects of climate warming change. Annu. Rev. Ecol. Evol. Syst. 37: 637–669.
on insects is the increase in voltinism (Yamamura and Kiritani 1998, Pinto, J. D. 2009. Hypermetamorphosis, pp. 484–486. In H. R. Vincent and
Matsuda et al. 2018). If climate change continues, individuals with R. T. Carde (eds.), Encyclopedia of Insects, 2nd ed. Academic Press, New
a bivoltine life cycle may increase in each population of E. gorhami. York, NY.
Selander, R. B., and J. M. Mathieu. 1964. The ontogeny of blister beetles
(Coleoptera, Meloidae) I. A study of three species of the genus Pyrota.
Acknowledgments Ann. Entomol. Soc. Am. 57: 711–732.
Shintani, Y., Y. Hirose, and M. Terao. 2011. Effects of temperature, photo-
This study was supported by JSPS KAKENHI (a Grant-in-Aid for period and soil humidity on induction of pseudopupal diapause in the
Encouragement of Scientists from the Ministry of Education, Culture, Sports, bean blister beetle, Epicauta gorhami. Physiol. Entomol. 36: 14–20.
Science and Technology of Japan) Grant Number JP17H00438. The research Shintani, Y., S. Tatsuki, and Y. Ishikawa. 1996. Geographic variation of
was part of a dissertation by the first author in partial fulfilment of a Ph.D. de- photoperiodic response in larval development of the yellow-spotted longi-
gree. All authors have provided consent for publication. We thank Kyosuke corn beetle, Psacothea hilaris (Pascoe)(Coleoptera: Cerambycidae). Appl.
Okuda (CTI AURA Co. Ltd.) for collecting the Kazo population of E. gorhami. Entomol. Zool. 31: 495–504.
Shintani, Y., M. Terao, and S. Tanaka. 2017. Adaptive significance of preco-
References Cited cious pupation in the bean blister beetle, Epicauta gorhami (Coleoptera:
Meloidae), a hypermetamorphic insect. J. Insect Physiol. 99: 107–112.
Andrew, N. R., S. J. Hill, M. Binns, M. H. Bahar, E. V. Ridley, M. P. Jung,
Tauber, M. J., and C. A. Tauber. 1972. Geographic variation in critical photo-
C. Fyfe, M. Yates, and M. Khusro. 2013. Assessing insect responses to
period and in diapause intensity of Chrysopa carnea (Neuroptera). J.
climate change: what are we testing for? Where should we be heading?
Insect Physiol. 18: 25–29.
PeerJ. 1: e11.
Tauber, M. J., C. A. Tauber, and S. Masaki. 1986. Seasonal adaptations of
Balduf, W. V. 1935 (reprinted 1969). The bionomics of entomophagous
insects. Oxford University Press, New York, NY.
Coleoptera. Hampton (Middx.): Classey.
Terao, M., Y. Hirose, and Y. Shintani. 2012. Effects of temperature and photo-
Boukal, D. S., A. Bideault, B. M. Carreira, and A. Sentis. 2019. Species
period on termination of pseudopupal diapause in the bean blister beetle,
interactions under climate change: connecting kinetic effects of tem-
Epicauta gorhami. J. Insect Physiol. 58: 737–742.
perature on individuals to community dynamics. Curr. Opin. Insect Sci.
Terao, M., Y. Hirose, and Y. Shintani. 2015. Food-availability dependent
35: 88–95.
premature metamorphosis in the bean blister beetle, Epicauta gorhami
Clausen, C. P. 1940. Entomophagous Insects. McGraw-Hill, NY and London.
(Coleoptera: Meloidae), a hypermetamorphic insect that feeds on
Danilevskii, A. S. 1965. Photoperiodism and seasonal development of insects.
grasshopper eggs in the larval stage. Entomol. Sci. 18: 85–93.
Oliver and Boyd, Edinburgh, United Kingdom.
Yamamura, K., and K. Kiritani. 1998. A simple method to estimate the po-
Danks, H. V. 1987. Insect dormancy: an ecological perspective. Biological
tential increase in the number of generations under global warming in
Survey of Canada, Ottawa, ON.
temperate zones. Appl. Entomol. Zool. 33: 289–298.You can also read
